Journal of Sea Research 63 (2010) 119–128

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Journal of Sea Research

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Facilitative effects of introduced Pacific on native macroalgae are limited by a secondary invader, the seaweed muticum

Anne C. Lang a, Christian Buschbaum b,⁎ a Institute of Ecology and Environmental Chemistry, Leuphana University Lüneburg, Scharnhorststr. 1, 21335 Lüneburg, Germany b Alfred Wegener Institute for Polar and Marine Research, Wadden Sea Station Sylt, Hafenstr. 43, 25992 List, Germany article info abstract

Article history: Introduced habitat-providing organisms such as epibenthic bivalves may facilitate the invasion and Received 17 June 2009 expansion of further non-native species which may modify the effects of the primary invader on the native Received in revised form 12 November 2009 system. In the sedimentary intertidal Wadden Sea (south-eastern ) introduced Pacific oysters Accepted 13 November 2009 (Crassostrea gigas) have overgrown native blue mussel beds (Mytilus edulis). These beds are now Available online 22 November 2008 providing the major attachment substratum for macroalgae. Recently, oysters have expanded their distribution into the shallow subtidal zone of the Wadden Sea, and there support a rich associated species Keywords: community including the Japanese seaweed Sargassum muticum, which has been presumably introduced Algal Canopy fi Epibenthos together with the oysters. With a block designed eld experiment, we explored the effects of S. muticum on Infauna the associated community of soft-bottom C. gigas beds in the shallow subtidal. Replicated oyster plots of − Introduced Species 1m2 were arranged with a density of 0, 7, 15 or 45 S. muticum m 2, respectively. We found no effects of Understorey Algae different S. muticum densities on associated epi- and endobenthic community compositions associated to the oyster plots. However, the overall coverage of sessile organisms settling on the oyster shells was significantly reduced at high S. muticum densities. The occurrence of abundant native macro-algal species such as Poly- siphonia nigrescens, Antithamnion plumula and Elachista fucicola decreased with increasing S. muticum densities. Sessile invertebrates, by contrast, were only marginally affected and we found no effects of S. muticum canopy on diversity and abundance of endofauna organisms. We conclude that increasing densities of S. muticum on C. gigas beds in the shallow subtidal zone of the Wadden Sea limit the occurrence of native macroalgae which otherwise would benefit from the additional hard substratum provided by the oysters. Thus, a secondary invader may abolish the effects of the primary invader for native species by occupying the new formed niche. © 2009 Elsevier B.V. All rights reserved.

1. Introduction down’ and may cause accelerated effects on recipient ecosystems (Simberloff and Von Holle, 1999). Introduced marine species can cause major effects on the recipient In addition to molluscs, macroalgae are regarded as important community by changing physical factors, community structure and habitat-providing invasive marine engineers (Reise et al., 2002; ecosystem properties (e.g. Callaway and Josselyn, 1992; Bruno, 2000; Gutiérrez et al., 2003; Schaffelke et al., 2006; Borthagaray and Grosholz et al., 2000; Crooks and Khim, 2002; Ruesink et al., 2006). Carranza, 2007; Schaffelke and Hewitt, 2007; Wallentinus and Jones et al. (1994) established the term ecosystem engineer for Nyberg, 2007; Buschbaum et al., 2009; Sousa et al., 2009). Non-native “species that modulate the availability of resources, by causing major algae may alter the recipient community by increasing structural changes in biotic and abiotic materials”. Coastal environments may be complexity that may enhance species richness and diversity (Crooks strongly affected if invasive species are ecosystem engineers that and Khim, 2002; Buschbaum et al., 2006). They may also affect algal provide new habitats in recipient systems (Crooks and Khim, 2002; and faunal understorey assemblages by modifying physical factors Cuddington and Hastings, 2004; Buschbaum et al., 2006; Wallentinus such as water flow (Velimirov and Griffiths, 1979; Eckman et al., 1989; and Nyberg, 2007; Sousa et al., 2009). The additional structures may Duggins et al., 1990; Russell, 2007), sedimentation rate (Eckman et al., facilitate the invasion of further non-native species. This positive 1989; Connell, 2005) and light conditions (Kennelly, 1989; Connell, interaction of non-indigenous species is termed ‘invasional melt- 2003; Toohey et al., 2004; Connell, 2005). In addition, sweeping algal fronds can affect other sessile organisms such as barnacles by scouring the substratum (Leonard, 1999; Irving and Connell, 2006). ⁎ Corresponding author. Tel.: +49 4651 956 4228; fax: +49 4651 956 4200. E-mail addresses: [email protected] (A.C. Lang), A very successful invasive alga is the Japanese seaweed Sargassum [email protected] (C. Buschbaum). muticum (Yendo) Fensholt (Phaeophyceae, ) which was first

1385-1101/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2009.11.002 120 A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128 described from and has currently an almost worldwide will further increase in the future. We hypothesized that S. muticum distribution (Critchley et al., 1990b). In the European Wadden Sea, coverage affects species abundance and diversity of an oyster bed and it was first detected in the western part near the island of Texel in that these effects depend on S. muticum density. To explore 1981 and reached the northern Wadden Sea in 1994 (Schories and these hypotheses we performed a field experiment with different Albrecht, 1996; Wolff, 2005). Reasons for its very efficient spreading S. muticum densities on experimental oyster plots. The aim was to are the physiological traits of the germlings (Hales and Fletcher, 1989) answer the following questions: (i) Does a S. muticum canopy affect and its high reproductive potential (Fletcher, 1980; Norton, 1981). the endobenthic community of an oyster bed? (ii) Does a S. muticum Germlings of S. muticum are tolerant to a wide range of salinities, canopy have an impact on the recruitment of sessile faunal and algal temperatures and light regimes (Hales and Fletcher, 1989). The alga is species settling on oyster shells? (iii) Do the effects depend on self-fertilizing and its fronds are breaking off in late summer serving S. muticum density? as floating vehicles for propagules (Fletcher, 1975, 1980; Norton, 1977, 1981). An additional dispersal vector is human mediated 2. Materials and methods transport with the Pacific oyster Crassostrea gigas (Thunberg) (Druehl, 1973; Critchley and Dijkema, 1984). The occurrence of S. muticum in 2.1. Study site an invaded area depends on the availability of hard substratum and is restricted by physical factors such as strong wave action, high Investigations and experiments were performed in a sheltered bay sedimentation rates and limited light conditions (Viejo et al., 1995; named “Königshafen” at the island of Sylt (54°55′N, 008°20′E) in the Thomsen, 2006). northern Wadden Sea (German Bight, North Sea) (Fig. 1). The bay is S. muticum has usually been considered an ecosystem engineer drained and flooded by a tidal creek. The semi-diurnal tides in this because it may influence a number of physical factors such as light area range up to 2 m. Mean water temperatures vary from 15 °C in conditions beneath dense seaweed canopies and might also affect summer to 4 °C in winter. Average salinity is 30 and maximum near- water flow, sedimentation rate, water temperature and nutrient bottom current velocities range between 0.3 and 0.5 m s− 1 (Austen, composition within algal beds (Critchley et al., 1990a,b; Britton- 1994a). Detailed descriptions of geology, hydrodynamics and sedi- Simmons, 2004; Strong et al., 2006; Domisch, 2008). These changes in ment composition in the area can be found in Bayerl and Higelke abiotic conditions may cause different effects on recipient algal (1994) and Austen (1994a,b). Further information on biota is given by assemblages (Olabarria et al., 2009; Sánchez and Fernández, 2005). Reise (1985), Reise et al. (1989, 1994) and Schories et al. (1997). Negative effects of S. muticum on diversity and abundance of native algal communities are reported from western Pacific coasts (from 2.2. Experimental design British Columbia through Washington State to California) and also from European coasts (Denmark, Scotland and Spain) (Ambrose and A field experiment was established to test the influence of Nelson, 1982; de Wreede, 1983; Viejo, 1997; Staehr et al., 2000; S. muticum canopies on oyster bed communities in the shallow Britton-Simmons, 2004; Harries et al., 2007). However, also facilitat- subtidal zone (0.3–0.5 m below mean low water tide level) of the ing effects on species numbers and diversity of less dominant algae of Wadden Sea. The experiment was set up on a sand flat in close an invaded assemblage were observed. For example, at the north coast proximity to an oyster bed where S. muticum naturally occurs (Fig. 1). of Spain (north-east Atlantic) Sánchez et al. (2005) found that Each experimental unit (plot) had a size of 1 m2 and consisted of 160 abundance of dominant native species may be reduced but total individuals of C. gigas collected from the oyster bed nearby (Fig. 2a). resident algal species number and diversity increased after establish- The oysters were carefully transplanted together with the associated ment of S. muticum. Similar to consequences of S. muticum species assemblage to ensure a natural community at the beginning of introduction on native algae the effects on resident benthic inverte- the experiment. Previous studies revealed that S. muticum density in brates may also be variable. On the Pacific coast of North America, for the study area is about 7–10 individuals m− 2 and remains stable from instance, invertebrate communities were not affected by S. muticum the end of April to October (Buschbaum et al., 2006; Polte and (Britton-Simmons, 2004) while at coasts of the Irish Sea and the Buschbaum, 2008). Experimental plots with four S. muticum density English Channel (north-east Atlantic) soft-bottom assemblages were treatments were established: (i) no S. muticum, (ii) density of different inside and outside S. muticum canopies (Strong et al., 2006). 7 individuals m− 2, (iii) density of 15 individuals m− 2 and (iv) a Consequently, effects of S. muticum introduction may be different and density of 45 individuals m− 2. Densities were kept constant during strongly depend on the considered variables in the native system the experimental period (end of April to October 2007) by adding (Williams and Smith, 2007). algal thalli when they were lost. We used density treatments instead In the sedimentary environment of the Wadden Sea, Buschbaum of coverage since cover is changing with ongoing seasonal growth of et al. (2006) revealed that S. muticum increases associated epibiota the S. muticum thalli. The four density treatments were arranged in a diversity because S. muticum provides a habitat which is much more randomized block design with 4 blocks each comprising 5 experi- structured than native macroalgae occurring in the area. However, for mental units. Each block contained every density treatment ensuring the area no studies exist that investigate the impacts of S. muticum on full orthogonality of the experiment which enabled us to test for block the habitat it is attached to. Shortly after its introduction, S. muticum effects (Fig. 2c). Additionally, each density treatment was replicated predominantly used epibenthic mussel beds of Mytilus edulis L. for in one of the blocks to test for possible interactions between recruitment which represented the major hard substratum available. treatment and block factor. However, within the last 5 years a dominance shift from native mussels to Pacific oysters C. gigas occurred and oyster shells are 2.3. Sampling representing today the dominant attachment substratum for S. muticum (Polte and Buschbaum, 2008). The rapid shift from mussel 2.3.1. Sessile organisms beds to aggregations dominated by oysters caused changes in the To test for effects of S. muticum on the recruitment of sessile associated species assemblage (Diederich et al., 2005; Kochmann species living attached to an oyster bed we chose oysters with a shell et al., 2008; Reise, 2008). In the shallow subtidal zone, this habitat is length of 150 to 160 mm from which we carefully removed all currently changing again because oyster beds become increasingly epibionts and used them as a recruitment matrix. Experiment overgrown by S. muticum. Therefore, this study focuses on the impacts beginning was two weeks after establishment of the plot at the end of S. muticum overgrowth on the associated species community of an of April 2007. For each plot 20 cleaned oysters were marked and oyster bed and investigates the scenario that S. muticum abundances randomly placed in the inner part (N20 cm from edge). After an A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128 121

Fig. 1. Study site (●) at the northern tip of the island of Sylt (German Bight, North Sea).

experimental period of 3 months (July 2007) and 6 months (October embedding plastic sticks for later fixation. The muffins were dried 2007), 10 marked oysters per plot were randomly sampled, for one week at 50 °C, fixedwiththeplasticstickstoironrodsusing respectively. Oysters were taken to the laboratory and sediment cable ties and then placed in the inner part of the experimental plots was carefully removed by rinsing them over a sieve. Afterwards, from September 28 to September 29, 2007. One gypsum muffinper sessile macroscopic algae and invertebrates were identified to species plot was positioned 10 cm above the bottom and thus right above the (or nearest possible taxonomic) level using a stereomicroscope. oysters. After 24 h (spanning two high tides and one low tide) For each oyster, percentage cover of all attached species was muffins were brought to the laboratory and weighted after being determined to the nearest 5%. Individual numbers of sessile faunal dried again (at 50 °C for 7 d). Weight loss was determined and used species (e.g. barnacles) were additionally counted and their abun- as a proxy of flow velocity in the treatments (method similar to dance oyster−1 determined. This was not done for macroalgae due to Eckman et al., 1989). difficulties in distinguishing single individuals in most species.

2.5. Sediment characteristics 2.3.2. Endobenthic organisms The infauna was sampled once in August 2007 during low tide. To test for effects of S. muticum overgrowth on sedimentation Samples were taken by using a tube corer of 5 cm of diameter within an oyster reef we determined sedimentation rate within the (sampling depth: 5cm). To compensate for a possible patchy experimental plots. Bottles with a volume of 500 ml, an opening distribution of organisms, six samples were randomly taken from diameter of 3.5 cm and a height of 21 cm were used as sediment traps. the inner part of each plot (N20 cm from edge, Fig. 2b) and pooled 3 The ratio of height to width of the used bottles was 6:1 and within the afterwards (total sample volume 98 cm ). Samples were washed over range recommended by Gardner (1980) for water velocities higher a sieve of 250 µm mesh size and organisms retained were counted and than 0.15 m s− 1. Flow velocity at our study area ranges from 0.3 to determined to species (or nearest possible taxonomic) level using a 0.5 m s− 1 (Austen, 1994a). For better handling each bottle was put in stereomicroscope. a PVC tube with a diameter of 10 cm which was placed randomly in the inner part of each plot. The opening of the tube was on the same 2.4. Water flow measurement height as the top of the oysters preventing oyster faeces from falling into the bottles. Additionally, the tube opening was covered with a net The relative near-bottom water velocity within the experimental (mesh size of 6 mm) to prevent mobile organisms such as crabs from plots was measured by means of weight loss of gypsum pieces. entering into the trap. Sediment was collected for 14 d from August 23 Gypsum (Bob Stone® DIN1168) was filled into muffinforms to September 5, 2007 spanning a neap-spring tidal period using one 122 A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128

Fig. 2. Experimental set-up. (a) Schematic drawing of an experimental plot with Crassostrea gigas covered by Sargassum muticum. (b) Experimental unit. Samples were only taken from the inner part to avoid edge effects. (c) Arrangement of the experimental plots in four blocks. sediment trap per plot. At the end of the experiment, trapped sediments were shaken in a stack of five sieves with decreasing sediment was washed with freshwater to remove salt and dried mesh sizes (mesh sizes: 1000, 600, 250, 125, and 63 µm) for 6min and afterwards. To analyse sediment grain size distribution the dry fractions were weighted to the nearest 0.1 g.

Fig. 3. MDS plots of species assemblages based upon Bray–Curtis similarities. (a) Endobenthic organisms (b) epibenthic organisms — July and (c) epibenthic organisms — October. A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128 123

2.6. Statistical analysis species between the treatments were detected (two-factorial ANOVA, pN0.05 for all species). Analysis of variance (ANOVA) was used to test for differences in The total number of epibenthic species was 33 with 19 macroalgae species abundances (epibionts and endofauna) and abiotic factors and 14 invertebrates in July and October 2007 (Table 2). In contrast to (flow velocity and sedimentation rate). The randomized block the endobenthic community, we detected effects of S. muticum on design was used to test for spatial heterogeneity between block epibenthic species occurrence. S. muticum density significantly affected sites. S. muticum density was used as a fixed factor and the block as epibenthic species number in July (two-factorial ANOVA, F3/13 =11.02, random factor. Interactions between block factor and treatments MS =10.24, p=0.001) (Fig. 4). Mean associated species number of showed no significance (pN0.05). Only in one case (effects of oyster plots without S. muticum (23.4±1.1) was significantly higher S. muticum occurrence on the abundance of B. crenatus in July) a than of plots with a S. muticum density of 15 ind.m−2 (20.6±1.3; significant effect was found (p=0.048) and we decided to neglect Tukey's test, p=0.015) and of 45 ind.m−2 (20.0±1.3; Tukey's test, interactions to enhance the power of the analysis (Underwood, 1997). p=0.008). Additionally, we detected a significant difference between All data were tested for homoscedasticity using Cochran's test. the mean species number of the treatment with 7 S. muticum ind.m−2 Abundance data needed to be log (x+1) transformed to fulfill (22.40±0.89) and the one with 45 ind.m−2 (Tukey's test, p=0.008).In homogeneity of variances. The post-hoc Tukey HSD test was used for October, however, no significant effect of S. muticum density on species comparisons between different S. muticum densities. number was detected (two-factorial ANOVA, F3/13=1.31, MS=4.46, Community analysis was conducted using multivariate, non- p=0.313). parametric ordination technique (Multidimensional Scaling) based The mean total percentage coverage of all epibiont species upon the Bray–Curtis similarity comparisons with the Primer TM oyster− 1 was also significantly affected by S. muticum density in software (Clarke and Warwick, 2001). For analyses of similarity (ANOSIM) of epibenthic communities we worked with percent − Table 2 coverage oyster 1 data while we used abundance data for the analyses List of sessile species detected in experimental treatments of different Sargassum of endobenthic communities. muticum densities (ind. m− 2) in July and October 2007. Results are presented as means with standard deviation. Effects were considered to be statistically significant if p-value was b0.05. Species July October 0 7 15 45 0 7 15 45

Algae 3. Results Chlorophyta Bryopsis lyngbyei Hornem. p p p p p p p p Chaetomorpha aerea (Dillwyn) Kützing p 3.1. Community responses Enteromorpha spp. Link p p c p p p p p Ulva spp. p p p p We detected no differences in the community composition between Phaeophyta treatments with different S. muticum density neither in the endobenthic Ectocarpus spp. Lyngb. p p p p p p p p (R-value of −0.278; pN0.05) nor in the epibenthic assemblage in July Elachista fucicola (Velley) Aresch. a a c c N − N Petalonia fascia (O.F.Müll.) O. Kuntze c c a a p p p p (R-value of 0.222; p 0.05) and October (R-value of 0.111; p 0.05) Sargassum muticum (Yendo) Fensholt c c c c (Fig. 3). Rhodophyta In total, we recorded 50 species in our experimental plots. In Acrochaetium spp. Nägeli p c c p August 2007, we found 17 endobenthic species with a dominance of Antithamnion plumula (Ellis) Thur. In Le Jolis c c c p c c c p Chondrus crispus Stackhouse p c p p p p p p Annelida and Mollusca (Table 1). Number of endobenthic species in Ceramium nodulosum (Lightf.) Ducluz. p p c p p p p p each treatment was 12 and no differences in the occurrence of single Dumontia incrassata (O.F. Müll) Lamour p c p p p Erythrotrichia spp. p p Polysiphonia nigrescens (Huds.) Grev. d a a a c c c p Polysiphonia violacea (Roth) Spreng. c c c p p p p p Table 1 Polysiphonia elongata (Huds.) Spreng. c c c p p p p p List of endobenthic species detected in experimental treatments of different Sargassum Porphyra sp. p p muticum densities (ind.m− 2) in August 2007. Fauna Species 0 7 15 45 Porifera Nemertea Halichondria panicea (Pallas) p p p c c c p Nemertini unidentified p p p Cnidaria Lineus ruber (Müller) p p Clytia hemispherica (L.) p Annelida Obelia longissima (Pallas) p p p p p p p p Aricidea minuta (Southward) c p p p Obelia geniculata (L.) p Capitella capitata (Fabricius) cccc Sagartiogeton undatus (Müller) a a a a p p p p Eulalia viridis (Linné) p p Sarsia tubulosa (M.Sars) p p p p p p p Malacoceros fuliginosus (Claparède) cccc Ciliophora Nereis diversicolor (O. F. Müller) p p Vorticella sp. p p p p p p p p Phyllodoce mucosa (Oersted) p Mollusca Scoloplos armiger (O. F. Müller) pppp Crepidula fornicata (L.) c c c c p c c c Tharyx killariensis (Southern) a a c a Lepidochitonia cinerea (L.) p c p p p p p p Tubificoides benedii (d' Udekem) dddd Crustacea Tubificoides pseudogaster (Dahl) dddd Elminius modestus Darwin a a c c d d a a Tubificoides sp. d d c d Balanus crenatus Bruguière d d d d a a a c Mollusca Semibalanus balanoides (L.) p p p p p p p p Mya arenaria (Linneus) p p Balanus improvisus Darwin p p p p p p p p Mysella bidentata (Montagu) p Tunicata Macoma balthica (Linneus) p Molgula manhattensis (de Kay) p p p p p p p p Venerupis sp. p p Styela clava Herdman p p p p p Total number of endobenthic species 17 12 12 12 12 Total number of epibenthic species 33 29 26 28 24 25 24 25 25

Semi-quantitative data on species abundances are given as mean individual counts per Semi-quantitative data on mean species occurrence are given as: p) present: b1% cover 98 cm3: p) present b1, c) common 1–5, a) abundant 6–10, d) dominant N10. oyster− 1; c) common: 1–5%; a) abundant: 6–9% and d) dominant ≥10%. 124 A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128

Fig. 4. Mean species number with standard deviation (+SD) (a) and mean percentage coverage (+SD) of all epibenthic species (b) at different Sargassum muticum densities in July and October. Significant differences are denoted as asterisks (pb0.05⁎, pb0.01⁎⁎).

both July (two-factorial ANOVA, F3/13 =8.47, MS=217.21, p=0.002) S. muticum and showed a decreasing trend with increasing S. muticum and October (F3/13 =4.43, MS=265.21, p=0.024)(Fig. 4). The overall densities in July (two-factorial ANOVA, F3/13 =6.76, MS=0.14, coverage was significantly reduced in plots with a S. muticum density of p=0.005). We detected a significant difference in E. fucicola coverage 45 ind.m−2 compared to the treatment without S. muticum (Tukey's between the treatment without and with 45 individuals m− 2 of test for July, p=0.011; and for October, p=0.001). In July, total mean S. muticum (Tukey's test p =0.013) (Fig. 5). Additionally, we coverage of epibenthic organisms oyster−1 decreased with increasing recognized a significant coverage difference of E. fucicola between algal density from 70.2% in the treatment without S. muticum to 50.1% in the treatment with seven S. muticum m− 2 and 45 individuals m− 2 plots with a S. muticum density of 45 ind.m−2 (Fig. 4). A similar (Tukey's test p=0.031). pattern was found in October with a decreasing total mean coverage Decreasing native algal coverage over the treatments with oyster−1 from 31.1% (without S. muticum)to12.3%(S. muticum density increasing S. muticum density per plot was also observed in the of 45 ind.m−2). species Chondrus crispus Stackh. and Dumonita contorta (Gmel.) Ruprecht. However, coverage in comparison to the above mentioned b − 1 3.2. Species responses macroalgae was low. Mean coverage was 1.5% oyster in the treatment with no S. muticum (treatment in which they achieved Considering species level we found a significant effect of highest coverage) and, thus, we decided not to test statistically. S. muticum density on the percent coverage oyster− 1 of the three Considering sessile faunal organisms, the most abundant species most abundant understorey algal species (Fig. 5). The mean coverage were the barnacles Balanus crenatus Bruguière and Elminius modestus −1 oyster− 1 of Polysiphonia nigrescens (Hudson) Greville ex. Harvey Darwin. Decreasing numbers in abundance oyster for both species was affected by S. muticum and significantly lower within the were observed between the treatments of increasing S. muticum treatments with S. muticum than without in both July (two-factorial density in July as well as in October (Table 3). However, results were not significant. Recruitment of all other sessile invertebrate species ANOVA, F3/13 =10.72, MS=0.08, p= 0.001) and October (two- was also not significantly affected by S. muticum. factorial ANOVA, F3/13 =3.90, MS=0.030, p=0.034). P. nigrescens showed the highest percent coverage of all algal species identified. In July, the coverage of Antithamnion plumula (J.Ellis) Thuret was 3.3. Water flow and sedimentation measurements also impaired by S. muticum and appeared to decrease with increasing

S. muticum density (two-factorial ANOVA, F3/13 =4.05, MS=0.11, The relative water flow velocity was indirectly quantified by p=0.031). Percentage coverage oyster− 1 was significantly different measuring weight loss of gypsum muffins. The density of S. muticum between the treatment without S. muticum and the treatment with a significantly affected water flow velocity (two-factorial ANOVA, F3/13 = S. muticum density of 45 ind.m− 2 (Tukey's test, p=0.045). No 5.71, MS=21.75, p=0.010). Within the treatment without S. muticum significant differences could be observed in October. water flow velocity was highest and significantly different from the Further, percentage coverage oyster− 1 of the brown alga Elachista treatment with 45 S. muticum individuals m−2 which showed the lowest fucicola (Velley) Aresch. was reduced within the treatments with water flow velocity (Tukey's test, p=0.004) (Fig. 6). A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128 125

Fig. 5. Effects of manipulated Sargassum muticum density on percent coverage oyster− 1 of understorey native algal species. Given are means with standard deviation (+SD). Significant results of the post-hoc Tukey test are denoted as asterisks (pb0.05⁎, pb0.01⁎⁎, pb0.001⁎⁎⁎).

We could not find any differences in sedimentation rate between with experimental oyster plots in the sedimentary environment of the the treatments of different S. muticum densities (Fig. 6). Neither the Wadden Sea. There were no significant effects of the S. muticum mean overall accumulated material per sediment trap (two-factorial canopy on community level. Additionally, no significant effects were

ANOVA, F3/13 =0.76, MS=271.82, p=0.54) nor a single sediment observed on the infauna. However, we detected significant effects of fraction of a certain grain size showed significant differences. S. muticum abundance on native understorey algae.

4. Discussion 4.1. Effects of S. muticum on endobenthic organisms

Using a small-scale field experiment we investigated the effects of A S. muticum canopy could have an impact on endobenthic organ- the invasive brown alga S. muticum on benthic organisms associated isms mediated by the change of physical factors. More specifically: the

Table 3 Mean densities oyster−1 (±SD) of the barnacles Balanus crenatus and Elminius modestus on experimental oyster reefs covered by different abundances of Sargassum muticum (ind.m−2)in July and October 2007.

July October

0 7 15 45 0 7 15 45

Balanus crenatus 82.5±45.3 65.5±20.2 68.5±28.9 65.8±19.8 25.1±12.4 20.7±5.2 18.0±9.2 11.9±3.1 Elminius modestus 28.7±7.8 33.6±13.3 21.0±8.1 17.9±7.1 61.1±12.4 49.9±31.3 32.5±14.1 28.9±19.4 126 A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128

Fig. 6. Effects of manipulated Sargassum muticum density on water velocity measured as mean weight loss (+SD) of exposed gypsum muffins (a) and on mean sedimentation (+SD) (b). Significant results of the post-hoc Tukey test are denoted as asterisks (pb0.05⁎).

canopy can reduce water velocity and, thus, indirectly may enhance The effect of S. muticum canopy on the coverage of native macroalgae sedimentation. However, contradictory effects of macro-algal coverage was significant for three abundant species: P. nigrescens, A. plumula on sedimentation are reported. Irving and Connell (2006) found (both Rhodophyta) and E. fucicola (Phaeophyta). The overall trend was reduced sedimentation beneath a canopy of Fucales. Eckman et al. similar: the percentage cover decreased with increasing S. muticum (1989), by contrast, found greater rates of particle deposition beneath density. Negative effects of S. muticum canopy on abundance of native understorey kelps. In case of S. muticum,however,neitherBritton- understorey algae in subtidal habitats was also found by Curiel et al. Simmons (2004), Strong et al. (2006) nor this study could detect any (1998) in the Mediterranean, by Staehr et al. (2000) in the North Sea and effect on sedimentation. An explanation that reduction of water velocity by Britton-Simmons (2004) in the eastern Pacific. did not have any effect on sedimentation rate in our experiment could The red macroalga P. nigrescens was the most dominant under- be the restricted plot area (1 m2). Particles that are slowed down above storey algal species on the experimental oyster plots and was strongly the plot would need some time to descend in the water column during affected by increased S. muticum densities in both July and October. which they are still transported by the current and they may touch the Similarly, Curiel et al. (1998) and De Wreede (1983) report negative ground somewhere outside the plot. However, we did not observe any effects of a S. muticum canopy on otherwise dominant species of the changes in sedimentation and sediment composition in the surrounding order Ceramiales, Rhodophyta. Interestingly, Buschbaum et al. (2006) area of the experimental plots. found that P. nigrescens grows as an epiphyte on S. muticum that may In contrast to the impacts of S. muticum on rocky shore communities, outweigh the reduction of P. nigrescens attached to C. gigas. However, investigations on the effects on soft-bottom communities are scarce. in contrast to the oysters, S. muticum only represents an ephemeral Strong et al. (2006) detected significant differences between the habitat because the thalli break off in autumn and float away together endobenthic assemblages underneath S. muticum canopy and those in with its associated species community. adjacent uncovered areas. They attribute the observed changes in The high occurrence of E. fucicola attached to oyster shells was not endobenthic assemblage to shading, flow suppression and temperature expected because this species is generally described as an epiphytic stratification. Our results, by contrast, revealed no effects of S. muticum macroalga mainly growing on Fucus-species. However, Kornmann canopy on infauna. In accordance to the results of Strong et al. (2006) and Sahling (1977) found that E. fucicola may also be very abundant this pattern can be explained by the experimental time period which on other substrates in the Wadden Sea. In October, E. fucicola was not was restricted to four months. However, Albrecht and Reise (1994) also found because its main growing season is limited from April to August show that the infauna associated with mussel beds of M. edulis in the in the area (Kornmann and Sahling, 1977). Wadden Sea was not affected by a heavy coverage with the bladder Reasons for algal coverage reduction below the S. muticum canopy wrack Fucus vesiculosus forma mytili (Nienburg) despite of an increased could be changes in physical factors. The detected reduction in water sedimentation rate. It is likely that the endobenthic organisms are more flow is unlikely to result in a difference of nutrient availability affected by the bivalves lying directly at the sediment surface than by between treatments because of the restricted plot size of 1 m2 in our the algal coverage above the bivalve beds. Görlitz (2005) and Kochmann experiment. Additionally, Britton-Simmons (2004) found no effect of et al. (2008), for example, show that aggregations of blue mussels S. muticum on nutrient availability for understory algae. Critchley et al. M. edulis beds and oysters C. gigas have different effects on the endo- (1990a) recognized a temperature stratification caused by the benthic community indicating that endobenthic organisms are strongly S. muticum canopy. However, incidental water temperature measure- influenced by the kind of bivalve species at the sediment surface. ments revealed no differences inside and outside S. muticum aggregations in our experimental plots. One important factor causing 4.2. Effects of S. muticum on sessile epibenthic organisms effects on other algae may be the reduction of light by S. muticum coverage and the importance of the shading effect of S. muticum Although we detected a significantly reduced species number of canopy was assumed by several authors (Curiel et al., 1998; Critchley epibionts on oyster beds as an effect of S. muticum coverage in July et al., 1990a; Britton-Simmons, 2004; Strong et al., 2006; Domisch, 2007 (but not in October) our results indicate that the differences in 2008). Similar to their results casual light measurements in our composition of an epibenthic soft-bottom oyster bed community in experiment showed that beneath S. muticum canopy light was less the Wadden Sea are small. However, we recognized a decrease of the than 5% of the uncovered plot at the same water depth. Since mean overall coverage of sessile species on oyster beds with S. muticum is a pseudoperennial species with only the holdfast S. muticum in both July and October 2007 which is caused by a persisting through the year the shading effect is restricted to spring reduction of native macroalgae. No significant effect on the abundance and summer (Norton, 1977). However, this is also the main growing of sessile benthic invertebrates could be detected. season for most native macroalgae occurring in the area. A.C. Lang, C. Buschbaum / Journal of Sea Research 63 (2010) 119–128 127

As shown for native macroalgae, S. muticum may also affect sessile Ambrose, R.F., Nelson, B.V., 1982. Inhibition of giant kelp recruitment by an introduced brown alga. Bot. Mar. 25, 265–267. benthic invertebrates recruiting and living below its canopy by Austen, G., 1994a. Hydrodynamics and particulate matter budget of Königshafen, mechanical disturbance of sweeping algal fronds (Jenkins et al., 1999; southeastern North Sea. Helgol. Mar. Res. 48, 183–200. Leonard, 1999; Connell, 2003) and reduction in light and water flow. A Austen, I., 1994b. The surficial sediments of Königshafen — variations over the past 50 years. Helgol. Mar. Res. 48, 163–171. light reduction favours the settlement of many invertebrate larvae that Bayerl, K.-A., Higelke, B., 1994. The development of northern Sylt during the Latest become photonegative at the end of their larval phase (Duggins et al., Holocene. Helgol. Mar. Res. 48, 145–162. 1990; Connell, 2003). Additionally, by the suppression of water flow a Bertness, M.D., Leonard, G.H., Levine, J.M., Schmidt, P.R., Ingraham, A.O., 1999. Testing depositional environment may emerge under the canopy where larval the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology 80 (8), 2711–2726. settlement is facilitated (Eckman et al., 1989; Leonard, 1999). Another Borthagaray, A.I., Carranza, A., 2007. Mussels as ecosystem engineers: their contribution to important effect which acts more indirectly is the enhanced consumer species richness in a rocky littoral community. Acta Oecologica 31, 243–250. pressure caused by the hiding opportunities beneath a canopy (Bertness Britton-Simmons, K.H., 2004. Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar. Ecol. Prog. et al., 1999). However, we obtained no data about predator abundance Ser. 277, 61–78. on the different plots. 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Pacific coast of North America. Levende Nat. 108 (2), 62–65. Callaway, J.C., Josselyn, M.N., 1992. The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries 15 (No 2), 218–226. 4.3. Conclusions Clarke, K.R., Warwick, R.H., 2001. Change in Marine Communities: An Approach to Statistical Analyses and Interpretation, 2nd ed. PRIMER-E Ltd, Plymouth, UK. The introduction of S. muticum to the Wadden Sea and its occurrence Connell, S.D., 2003. Negative effects overpower the positive of kelp to exclude invertebrates from the understory community. Oecologia 137, 97–103. on soft-bottom oyster beds may cause different effects. Epibenthic and Connell, S.D., 2005. Assembly and maintenance of subtidal habitat heterogeneity: endobenthic community composition at oyster aggregations seem to be synergistic effects of light penetration and sedimentation. Mar. Ecol. Prog. Ser. 289, not affected while single native algal species show a decrease in 53–61. abundance. Additionally, S. muticum provides habitat for a rich epibiont Critchley, A.T., Dijkema, R., 1984. On the presence of the introduced brown alga Sargassum muticum,attachedtocommerciallyimportedOstrea edulis in the S.W. . species community associated with the algal thalli (Buschbaum et al., Bot. Mar. 27, 211–216. 2006). The ongoing dispersal of C. gigas and its spread into the shallow Critchley, A.T., De Visscher, P.R.M., Nienhuis, P.H., 1990a. Canopy characteristics of the subtidal zone of the Wadden Sea result in a marked augmentation of brown alga Sargassum muticum (Fucales, Phaeophyta) in Lake Grevelingen, southwest Netherlands. Hydrobiologia 204 (205), 211–217. biogenic hard substrate in an environment otherwise dominated by Critchley, A.T., Farnham, W.F., Yoshida, T., Norton, T.A., 1990b. A bibliography of the unstable sediments. 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